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Rossi, F.;  Giaccone, V.;  Colavita, G.;  Amadoro, C.;  Pomilio, F.;  Catellani, P. Listeria ivanovii. Encyclopedia. Available online: https://encyclopedia.pub/entry/26390 (accessed on 14 May 2024).
Rossi F,  Giaccone V,  Colavita G,  Amadoro C,  Pomilio F,  Catellani P. Listeria ivanovii. Encyclopedia. Available at: https://encyclopedia.pub/entry/26390. Accessed May 14, 2024.
Rossi, Franca, Valerio Giaccone, Giampaolo Colavita, Carmela Amadoro, Francesco Pomilio, Paolo Catellani. "Listeria ivanovii" Encyclopedia, https://encyclopedia.pub/entry/26390 (accessed May 14, 2024).
Rossi, F.,  Giaccone, V.,  Colavita, G.,  Amadoro, C.,  Pomilio, F., & Catellani, P. (2022, August 23). Listeria ivanovii. In Encyclopedia. https://encyclopedia.pub/entry/26390
Rossi, Franca, et al. "Listeria ivanovii." Encyclopedia. Web. 23 August, 2022.
Listeria ivanovii
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This entry is adapted from the peer-reviewed paper 10.3390/microorganisms10081679

Listeria ivanovii invasiveness, pathogenicity and distribution in the environment.

Listeria ivanovii pathogenicity virulence characters

1. L. ivanovii Invasiveness

The cell invasion capacity of L. ivanovii was demonstrated for different host cell types of human and animal origin.
Guillet et al. [1] reported that the L. ivanovii isolates from a patient with gastroenteritis and bacteremia were hyperinvasive in Madin-Darby bovine kidney (MDBK) cells, even more than L. monocytogenes, and less invasive in HeLa cells. They also performed invasion assays with cells expressing or not human E-cadherin that did not show substantial differences in invasiveness for the two different cell types, suggesting that L. ivanovii InlA does not interact with E-cadherin.
Alvarez-Ordóñez et al. [2] showed, by cell invasion assays, that the majority of L. ivanovii strains had comparable ability to invade CaCo-2 epithelial cells with L. monocytogenes EGDe, while four isolates had even higher invasion efficiencies.
Ammendolia et al. [3] demonstrated that L. ivanovii is able to adhere to human amniotic cells, invade the cytoplasm, lyse the phagosome, synthetize actin tails and spread among adjacent cells as efficiently as L. monocytogenes. However, L. ivanovii showed a lower survival capacity in the host cell cytoplasm compared to L. monocytogenes.
Rocha et al. [4], using L. ivanovii type strain ATCC 19119, demonstrated for the first time the susceptibility of bovine trophoblastic cells to L. monocytogenes and L. ivanovii, that can explain the abortions and reproductive failures caused by L. ivanovii in cattle.
Gan et al. [5] reported high invasion ability, cytotoxicity and intracellular growth in CaCo-2 and MDBK cells for a L. ivanovii ST1 strain. Growth in cells appeared from 3 to 6 h post-infection in both cell types. This strain caused a remarkable weight loss and injuries in liver and spleen in an intraperitoneal infection trial in mice.
In a study carried out in vivo in mice the invasiveness of L. ivanovii appeared to be much lower than that of L. monocytogenes. In mice intravenously inoculated with 5 × 105 CFU of L. ivanovii PAM 55, about 88% of the bacteria invaded liver and decreased gradually. Lesions were few but large and consisted of layers of necrotic hepatocytes and lymphocytes. The load of L. ivanovii in the spleen and in the lung decreased to below the detection limit after 3 days post infection (dpi) and no lesions were observed in spleens, thus showing a limited ability of the strain to maintain infection. In the lung collapsed alveoli accompanied with lymphocytes appeared.
After intranasal inoculation, L. ivanovii was localized in the lung, where it remained at high loads until 5 dpi and then dropped sharply, while liver and spleen were invaded very little. Tissue damage of the lungs was severe but with lesions densely packed, indicating a limited ability of L. ivanovii to enlarge the infection foci. The hepatic lesions were small and splenic necrosis was hardly observed [6].
In an experimental infection of broiler chicken with 1.5 × 108 CFU of L. ivanovii UNCSM–042, isolated in Ukraine, post-mortem examination after 23 dpi allowed to observe an enlargement of the spleen, an overfilled gallbladder, congestive hyperemia of the internal organs, and hyperplasia of the intestinal vessels. However, the growth level of the infected animals was not affected compared to the controls [7]. Based on the available evidences, limited invasiveness in vivo can account for the rare occurrence of L. ivanovii infections.

2. L. ivanovii Persistence and Tolerance to Harsh Conditions

Environmental persistence of Listeria spp. is determined by the capacity of these bacteria to form biofilms. Nyenje et al. [8] investigated the biofilm forming capacity of L. ivanovii strains and observed that 88% of the strains were able to form biofilm at 25 °C with four biofilm phenotypes. This indicated the ability of the L. ivanovii species to adhere at room temperature to surfaces and utensils not properly cleaned, from which it can contaminate food. A high persistence capacity of L. ivanovii was indeed reported for a cheese production plant where the same pulsed field gel electrophoresis (PFGE) AscI and ApaI pulsotype of L. ivanovii was isolated over a six-month period [9].
Determinants conferring resistance to cadmium and arsenic are widely distributed among Listeria species and an association was observed between resistance to cadmium and resistance to benzalkonium chloride, a sanitizer commonly used in food industries. To date, six cadmium efflux systems have been described in Listeria spp. that are located on transposons inserted in plasmids or within integrative conjugative elements (ICE) in the chromosome. It was observed that the presence of some cadAC resistance cassettes in Listeria spp. can influence virulence and biofilm formation. Among the cadmium resistance determinants described to date, cadA6b was found to be encoded by the L. ivanovii plasmid pLIS6, the first plasmid characterized for this species, in which the cadA6b cassette was probably introduced via a 6-kb non-composite transposon [10]. Resistance of L. ivanovii to benzalkonium chloride was directly investigated in a study regarding the distribution of the Tn6188 transposon of L. monocytogenes, encoding the multidrug resistance transporter QacH, in other Listeria species, and it was found that the ten L. ivanovii strains considered did not harbor this transposon [11].
In another study it was observed that two L. ivanovii strains isolated from postharvest sources in fresh produce processing could adapt to levels of benzalkonium chloride 3-fold higher than non-adapted wild types for the arising of nonsense mutations in the fepR regulator gene of the fepRA operon, which encodes the efflux pump FepA [12].
The tolerance to low pH values was analyzed in relation to the cell invasion capacity and at different levels of iron availability. L. ivanovii subsp. ivanovii ATCC 19119 was not able to grow at pH 5.1 and exposure to this pH did not trigger an acid tolerance response (ATR) for adaptation to lower pH values. Indeed, the bacterium was rapidly killed at pH 3.5. Acid-adapted cells showed a higher percentage of internalization in CaCo-2 cells when iron was added to the culture medium. Iron depletion enhanced the capacity of the bacterium to invade amniotic cells, regardless of acid adaptation or not [13].

3. Environmental Distribution of L. ivanovii

Investigations on the distribution of L. ivanovii in the environment mainly regarded its presence in animals and it was isolated from mastitis cases in cattle and buffalo [14], from aborted goats (7.5%), mastitic goats (5.6%) and healthy goats (14.5%) [15].
Studies carried out in China indicated that wild rodents could represent a reservoir of bacteria belonging to the species L. ivanovii, though the isolation of this species was not frequent. Among 341 intestinal fecal samples of rodents captured from five different regions of China, seven were positive for L. ivanovii. All of these came from animals captured in Tibet; five at the junction of farm area and woodland and two in grasslands. Three isolates derived from A. peninsulae, two from Cricetulus kamensis and two from N. confucianus [16]. Cao et al. [17] isolated 26 L. ivanovii strains from 702 fecal samples of 25 different species of wild rodents from six provinces of China. The isolates were assigned to 5 STs with ST6 being the dominant type. The prevalence of L. ivanovii was higher in some regions, and the genetic diversity was relatively low since most isolates belonged to one lineage.
In an investigation carried out in Turkey, L. ivanovii was isolated from the abomasum content of an aborted fetus from a farm with history of silage feeding, among 538 analyzed specimens comprising 229 milk samples, 263 vaginal swabs and 46 abomasum contents of aborted sheep fetuses. In another sample of abomasum content from an aborted fetus L. ivanovii was identified by direct application of genus-specific PCR and subsequent 16S rRNA gene sequencing [18].
Abuhatab et al. [19] reported that L. ivanovii was the most prevalent species isolated from cloacal swabs of avian species in a study carried out in Egypt. This species was found in 32% samples from broilers, layers, pigeons, ducks and turkeys and was isolated from all these animals. Moreover, it was isolated from two of eight chicken carcasses, one of four chicken luncheons, one of three frozen chicken breast fillets, 2 of 9 eggshells and one of two fecal specimens from poultry farm workers. Molecular identification tests were carried out only for the L. monocytogenes isolates. This entry suggested to further investigate the occurrence of L. ivanovii in avian species.
In an investigation carried out in all the operational units of an Ethiopian university dairy farm, L. ivanovii, identified on the basis of biochemical tests, was not isolated from feed (silage) but from the milk harvesting cylinder, pooled milk at collection and supply and milk measuring equipment in one or two out of 10 samples. It could not be isolated from cow barn and milking parlor floors, drinking and cleaning water and teat drying towels. Therefore, it is possible that the milk harvesting cylinder was contaminated by a persistent L. ivanovii strain that was released into the milk [20].
In Latvia, L. ivanovii was isolated from 2 among 136 water samples from river and farm water and 3 of 111 animal feces samples in cattle farms [21].
Deer and wild boars were indicated as natural reservoirs of L. ivanovii in a study in which the subsp. londoniensis was detected in 4 among 23 tonsil samples [22].
In an analysis of Listeria sensu stricto species distribution in publicly available metagenomic datasets from the large MG-RAST database, 11,907 16S rRNA sequence high-quality datasets were examined [23]. L. ivanovii specific sequences were detected in soil, human and animal hosts, sludge and sediments. It was the second abundant species in humans, particularly in datasets from gut and skin, cow and goat associated environments. This finding indicates that the culture-dependent examination allows the isolation of L. ivanovii only from a subset of samples in which it is present. In addition, only L. ivanovii was detected in 16S rRNA datasets from goats, confirming the association of L. ivanovii with small ruminants [24].

References

  1. Guillet, C.; Join-Lambert, O.; Le Monnier, A.; Leclercq, A.; Mechai, F.; Mamzer-Bruneel, M.F.; Bielecka, M.K.; Scortti, M.; Disson, O.; Berche, P.; et al. Human listeriosis caused by Listeria ivanovii. Emerg. Infect. Dis. 2010, 16, 136–138.
  2. Alvarez-Ordóñez, A.; Leong, D.; Morgan, C.A.; Hill, C.; Gahan, C.G.; Jordan, K. Occurrence, persistence, and virulence potential of Listeria ivanovii in foods and food processing environments in the Republic of Ireland. BioMed. Res. Int. 2015, 2015, 350526.
  3. Ammendolia, M.G.; Superti, F.; Bertuccini, L.; Chiarini, F.; Conte, M.P.; Cipriani, D.; Seganti, L.; Longhi, C. Invasive pathway of Listeria ivanovii in human amnion-derived WISH cells. Int. J. Immunopathol. Pharmacol. 2007, 20, 509–518.
  4. Rocha, C.E.; Mol, J.P.S.; Garcia, L.N.N.; Costa, L.F.; Santos, R.L.; Paixao, T.A. Comparative experimental infection of Listeria monocytogenes and Listeria ivanovii in bovine trophoblasts. PLoS ONE 2017, 12, e0176911.
  5. Gan, L.; Mao, P.; Jiang, H.; Zhang, L.; Liu, D.; Cao, X.; Wang, Y.; Wang, Y.; Sun, H.; Huang, Y.; et al. Two prevalent Listeria ivanovii subsp. ivanovii clonal strains with different virulence exist in wild rodents and pikas of China. Front. Vet. Sci. 2020, 7, 88.
  6. Zhou, M.; Jiang, M.; Ren, C.; Liu, S.; Pu, Q.; Goldfine, H.; Shen, H.; Wang, C. Listeria ivanovii Infection in Mice: Restricted to the Liver and Lung with Limited Replication in the Spleen. Front. Microbiol. 2016, 7, 790.
  7. Borovuk, I.; Zazharska, N. Evaluation of broiler meat in experimental listeriosis. J. Adv. Vet. Anim. Res. 2022, 9, 155–165.
  8. Nyenje, M.E.; Green, E.; Ndip, R.N. Biofilm formation and adherence characteristics of Listeria ivanovii strains isolated from ready-to-eat foods in Alice, South Africa. Scient. World J. 2012, 2012, 873909.
  9. Vázquez-Villanueva, J.; Orgaz, B.; Ortiz, S.; López, V.; Martínez-Suárez, J.V.; Sanjose, C. Predominance and persistence of a single clone of Listeria ivanovii in a Manchego cheese factory over 6 months. Zoonoses Public Health 2010, 57, 402–410.
  10. Chmielowska, C.; Korsa, D.; Szmulkowska, B.; Krop, A.; Lipka, K.; Krupińska, M.; Bartosik, D. Genetic Carriers and Genomic Distribution of cadA6-A Novel Variant of a Cadmium Resistance Determinant Identified in Listeria spp. Int. J. Mol. Sci. 2020, 21, 8713.
  11. Müller, A.; Rychli, K.; Zaiser, A.; Wieser, C.; Wagner, M.; Schmitz-Esser, S. The Listeria monocytogenes transposon Tn6188 provides increased tolerance to various quaternary ammonium compounds and ethidium bromide. FEMS Microbiol. Lett. 2014, 361, 166–173.
  12. Bolten, S.; Harrand, A.S.; Skeens, J.; Wiedmann, M. Nonsynonymous Mutations in fepR Are Associated with Adaptation of Listeria monocytogenes and Other Listeria spp. to Low Concentrations of Benzalkonium Chloride but Do Not Increase Survival of L. monocytogenes and Other Listeria spp. after Exposure to Benzalkonium Chloride Concentrations Recommended for Use in Food Processing Environments. Appl. Environ. Microbiol. 2022, 88, e0048622.
  13. Longhi, C.; Ammendolia, M.G.; Conte, M.; Seganti, L.; Iosi, F.; Superti, F. Listeria ivanovii ATCC 19119 strain behaviour is modulated by iron and acid stress. Food Microbiol. 2014, 42, 66–71.
  14. Rawool, D.B.; Malik, S.V.S.; Shakuntala, I.; Sahare, A.M.; Barbuddhe, S.B. Detection of multiple virulence-associated genes in Listeria monocytogenes isolated from bovine mastitis cases. Int. J. Food Microbiol. 2007, 113, 201–207.
  15. Elezebeth, G.; Malik, S.V.S.; Chaudhari, S.P.; Barbuddhe, S.B. The occurrence of Listeria species and antibodies against listeriolysin-O in naturally infected goats. Small Rumin. Res. 2007, 67, 173–178.
  16. Wang, Y.; Lu, L.; Lan, R.; Salazar, J.K.; Liu, J.; Xu, J.; Ye, C. Isolation and characterization of Listeria species from rodents in natural environments in China. Emerg. Microbes Infect. 2017, 6, e44.
  17. Cao, X.; Wang, Y.; Wang, Y.; Li, H.; Luo, L.; Wang, P.; Zhang, L.; Li, H.; Liu, J.; Lu, L.; et al. Prevalence and Characteristics of Listeria ivanovii Strains in Wild Rodents in China. Vector Borne Zoonotic Dis. 2019, 19, 8–15.
  18. Akca, D.; Buyuk, F.; Celik, E.; Saglam, A.G.; Otlu, S.; Dag, S.; Celebi, O.; Coskun, M.R.; Buyuk, E.; Karakurt, E.; et al. Phylogenetic positioning of Listeria ivanovii identified in aborted sheep in Kars Region (Turkey). Thai J. Vet. Med. 2022, 52, 145–150.
  19. Abuhatab, E.; Naguib, D.; Abdou, A.; Gwida, M.; Elgohary, A. Genetic Characterization and Antibiogram Profiles of Listeria species Isolated from Poultry and Poultry Handlers. J. Adv. Vet. Res. 2022, 12, 205–210.
  20. Ahimeda, H.M.; Hikoa, A.; Abdellaha, A.; Muktarb, Y.D.; Gutema, F.D. Isolation and multidrug drug resistance profile of Listeria species in selected Dairy Farm’s Operational stages in Oromia Regional State, Ethiopia. Sci. Afr. 2022, 16, e01167.
  21. Terentjeva, M.; Šteingolde, Z.; Meistere, I.; Elferts, D.; Avsejenko, J.; Streikiša, M.; Gradovska, S.; Alksne, L.; Ķibilds, J.; Bērziņš, A. Prevalence, Genetic Diversity and Factors Associated with Distribution of Listeria monocytogenes and Other Listeria spp. in Cattle Farms in Latvia. Pathogens. 2021, 10, 851.
  22. Palacios-Gorba, C.; Moura, A.; Leclercq, A.; Gómez-Martín, A.; Gomis, J.; Jiménez-Trigos, E.; Mocé, M.L.; Lecuit, M.; Quereda, J.J. Listeria spp. Isolated from Tonsils of Wild Deer and Boars: Genomic Characterization. Appl. Environ. Microbiol. 2021, 87, e02651–e02720.
  23. Meshref, L.; Pichon, M.; Burucoa, C.; Nusser, S.H.A.; Moura, A.; Garcia-Garcera, M.; Lecuit, M. Listeria monocytogenes faecal carriage is common and depends on the gut microbiota. Nat. Commun. 2021, 12, 6826.
  24. Ramage, C.P.; Low, J.C.; McLauchlin, J.; Donachie, W. Characterisation of Listeria ivanovii isolates from the UK using pulsed-field gel electrophoresis. FEMS Microbiol. Lett. 2006, 170, 349–353.
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Subjects: Microbiology
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
Franca Rossi
,
Valerio Giaccone
,
Giampaolo Colavita
,
Carmela Amadoro
,
Francesco Pomilio
,
Paolo Catellani
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Revisions: 2 times (View History)
Update Date: 30 Aug 2022
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